Intestinal parasites in a population of stone marten (Martes foina) in central Spain

Olmedo, C.Refoyo, P.García, D.Muñoz, B.

Abstract

Intestinal parasites in a population of stone marten (Martes foina) in central SpainTwenty-one fresh fecal samples from stone marten (Martes foina) (Erxleben, 1777) collected in the Natural Park of Hoces del Río Riaza (Segovia) were processed using a modified version of Ritchie’s concentration method. We identified 18 genera: four coccidian; two trematodes; three cestodes; eight nematodes; and one acanthocephalan. The prevalence was low for all genera except Isospora sp. (Schneider, 1875), Eimeria sp. (Schneider, 1875) and Toxocara sp. (Stiles, 1905) that showed values above 20 %. The richness of parasites was lower than that detected in other populations, and it is likely that the stone martens help disseminate these parasites as their external appearance was good.

The aim of this study was to analyze the intestinal parasite burden in the stone marten (Martes foina) in a protected area in the centre of the Iberian peninsula and to identify possible differences with species in other areas of the Iberian peninsula and Europe. We also aimed to analyze the prevalence of these diverse parasites.

Geographically, the study area is nestled in the Mediterranean region, in the lower supra-Mediterranean zone that has almost nine months a year of probable frosts and four months of drought (Rivas Martínez, 2007). The varied topography of the area, its limestone formation and the region’s economic exploitation are the determinant factors of the presence of this diverse vegetation formed by juniper, holm oak and Portuguese oak trees. The rest of the vegetation in the area consists of riparian forest at the bottom of the valley with communities of scrubland, grassland and aquatic species, besides the existence of a major area of rain fed crops, and to a lesser extent, of irrigation in the meadow of the river Riaza.

Methods

We obtained 21 fecal samples from stone marten (Martes foina) collected along a fixed itinerary from Valdevacas to the Riaza river within the Natural Park of Hoces del Río Riaza (Segovia) using photo-trapping with DLC-Covert 2 cameras in 58 previously established catchment areas. We considered the habitat requirements of the species as well as the distance to water points, vegetation cover and type of land management (Park area vs authorized area) using the existing government layers in GIS (www.esri.com). The cameras were installed in November 2013 and were active at each point for 5 days. Each capture zone was baited with cans of sardines and the cameras were programmed to emit bursts of three photos at 20-second intervals. These capture areas were separated from each other by at least 1 km. We only selected the faeces identified by experienced observers as fresh samples of stone marten in the areas where presence of the species was confirmed through camera traps and where no other species with similar faeces were present (Davison et al., 2002). Fecal samples were placed in plastic bags, labelled and sealed for shipment and storage in the laboratory where they remained refrigerated for a maximum of 24 hours at 4 °C to prevent the growth of fungi. We then maintained the samples in potassium dichromate (3.5 %) for seven days to enhance the sporulation of oocysts. Next, we took 3 g of each sample for later concentration and the remaining samples were placed in 10 % formalin to fixation for re-use if necessary.

Due to the morphological similarity of some eggs, we were unable to clearly distinguish between them using only the diagnostic methods applied in this study so we also compared them with the collection of parasites of the Department of Biodiversity, Ecology and Evolution of the Faculty of Biological Sciences of the Universidad Complutense de Madrid. Regarding prevalence, coccidia and nematodes were found in 61.9 % of the samples, cestodes in 23.81%, trematodes in 19.05 %, and acanthocephalan in 4.76 %. (table 1).

Isospora sp. and Eimeria sp. showed the highest prevalence within the coccidia (table 1). Among the helminths, nematodes were the most abundant taxon, and within these, Toxocara sp. Among cestodes, the most abundant taxon were Oochoristica sp. and Taenia sp. with a prevalence of 15 to 20 %, and the prevalence of Troglotrema sp. was 14.29 % among trematodes. Acanthocephala was the only Centrorhyncus sp. found (table 1).

Only five of the analyzed samples were free of parasites (23.81 %). Taking the samples with parasites into account, 10 of the samples had more than one parasite, and sample I10 had 12 different parasites (table 2).

Discussion

Analysis of fecal samples limits the parasites obtained to particular groups (related with the digestive tract) and to certain stages of those parasites (cysts, eggs, larvae). It does not allow specific determination without further genetic studies. These analyses are usually a standard procedure in the study of parasites because sampling is much simpler (it is not necessary to capture the specimen), the variety of parasitic species is sufficiently high, and relative specificity is low, and identification to genus is relatively simple (Painer et al., 2011; Pfukenyi et al., 2007). The species of coccidia are identified after sporulation (Levine 1985).

Although the stone marten is common in the Iberian peninsula, studies concerning its intestinal parasite fauna are few. At a European level, 30 different species of parasites have been related to this mustelid (Aubry et al., 2012). In this study, we confirmed the presence of 18 genera previously reported in the literature.

Comparison of results with those from studies in the literature showed several differences. The prevalence of coccidia was higher in our study (61.9 %), but comparison is difficult in view of the few references found and the low number of samples in the study ofRodríguez and Carbonell (1998) (n = 4). Focusing on the helminth fauna, the most studied group to date, and comparing our data with those from Miquel (1993) and Miquel et al. (1994a, 1994b), we found that prevalences were lower in our studies for all analyzed genera, except for Uncinaria sp. and Baylisascaris sp., (in both cases with values of 14.29 % compared to their 1.98 % or the 25 % of Di Cerbo et al. (2008) in Uncinaria sp.). Findings from other studies were also higher for the genera Eucoleus sp. (34 compared to our 19.05 %) and Personema sp. (22 % vs our 4.76 %). When comparing the values of Taenia sp. of Di Cerbo et al. (2008) we find a lower percentage (12.5 % compared to our 19.05 %) but the prevalence of Aonchoteca sp. was higher (22.2 % vs our 4.76 %). The explanation for these differences may be the type of the sample and lower number of samples in our study. Neither can it be ruled out that the harsh environmental conditions in this area compared to the Mediterranean areas may play a role (Miquel et al., 1994b; Rosalino et al., 2011). External environmental conditions have been found to be indispensable for the survival of helminths (Kates, 1965) and protozoa (Schustera and Visvesvara, 2004), especially when frosts occur (Robertson et al., 1992), a frequent circumstance in the study area.

All the parasites found have a low host specificity and are common in several families of wild carnivores, probably due to their similar diet composition (Miquel et al., 1994b; Ribas et al., 2004). The lower parasite richness detected in comparison with other populations and the good external appearance of the observed specimens may indicate that the stone martens help to disseminate these parasites in wild carnivores.

Acknowledgements

This work was possible thanks to the contribution of José Luis Tellería, Guillermo Fandos, and Javier Fernández, who facilitated and placed the cameras for the camera trapping.